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Gąsiorowski and Hejnol EvoDevo (2019) 10:1 https://doi.org/10.1186/s13227-018-0114-1 EvoDevo RESEARCH Open Access Hox gene expression in postmetamorphic juveniles of the brachiopod Terebratalia transversa Ludwik Gąsiorowski and Andreas Hejnol* Abstract Background: Hox genes encode a family of homeodomain containing transcription factors that are clustered together on chromosomes of many Bilateria. Some bilaterian lineages express these genes during embryogenesis in spatial and/or temporal order according to their arrangement in the cluster, a phenomenon referred to as collinear- ity. Expression of Hox genes is well studied during embryonic and larval development of numerous species; however, relatively few studies focus on the comparison of pre- and postmetamorphic expression of Hox genes in animals with biphasic life cycle. Recently, the expression of Hox genes was described for embryos and larvae of Terebratalia transversa, a rhynchonelliformean brachiopod, which possesses distinct metamorphosis from planktonic larvae to sessile juveniles. During premetamorphic development, T. transversa does not exhibit spatial collinearity and several of its Hox genes are recruited for the morphogenesis of novel structures. In our study, we determined the expression of Hox genes in postmetamorphic juveniles of T. transversa in order to examine metamorphosis-related changes of expression patterns and to test whether Hox genes are expressed in the spatially collinear way in the postmetamor- phic juveniles. Results: Hox genes are expressed in a spatially non-collinear manner in juveniles, generally showing similar patterns as ones observed in competent larvae: genes labial and post1 are expressed in chaetae-related structures, sex combs reduced in the shell-forming epithelium, whereas lox5 and lox4 in dorso-posterior epidermis. After metamorphosis, expression of genes proboscipedia, hox3, deformed and antennapedia becomes restricted to, respectively, shell muscu- lature, prospective hinge rudiments and pedicle musculature and epidermis. Conclusions: All developmental stages of T. transversa, including postmetamorphic juveniles, exhibit a spatial non- collinear Hox genes expression with only minor changes observed between pre- and postmetamorphic stages. Our results are concordant with morphological observation that metamorphosis in rhynchonelliformean brachiopods, despite being rapid, is rather gradual. The most drastic changes in Hox gene expression patterns observed during metamorphosis could be explained by the inversion of the mantle lobe, which relocates some of the more posterior larval structures into the anterior edge of the juveniles. Co-option of Hox genes for the morphogenesis of novel struc- tures is even more pronounced in postmetamorphic brachiopods when compared to larvae. Keywords: Metamorphosis, Hox gene collinearity, Indirect development, Morphology, Spiralia, Lophophorata, Biphasic life cycle *Correspondence: [email protected] Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat​iveco​mmons​.org/ publi​cdoma​in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Gąsiorowski and Hejnol EvoDevo (2019) 10:1 Page 2 of 19 Background of the Hox genes, yet there are shifts in the combinations Hox genes encode a family of conserved homeodomain of genes defning particular body regions before and after transcription factors from the ANTP class, which by metamorphosis [47, 48]. On the other hand, in other ani- binding to regulatory DNA sequences can activate or mals (especially those with the more pronounced meta- suppress transcription of downstream genes (e.g., [1, 2]). morphosis) only one of the developmental stages exhibits Hox genes are present in genomes of almost all investi- canonical spatial collinearity of Hox genes expression, gated animals (with exception of Porifera, Ctenophora whereas the remaining stage shows either a non-col- and Placozoa [3–7]) and are hypothesized to represent linear expression or does not express Hox genes at all. a synapomorphy of the clade consisting of Cnidaria and For instance, in the tunicate Ciona intestinalis Hox genes Bilateria [4, 8–10]. In most of bilaterians, Hox genes exhibit spatially collinear expression in the nervous sys- are expressed during embryogenesis, being involved in tem of larvae, whereas in juveniles only the three poste- antero-posterior (A-P) patterning of either the whole rior genes are expressed in the intestine [15]. Conversely embryo or at least some of its developing organ systems in pilidiophoran nemertean Micrura alaskensis and in (e.g., [1, 2, 11]). Interestingly, in the genomes of some indirectly developing enteropneust Schiozcardium cali- animals, the Hox genes are clustered along the chromo- fornicum the specialized larvae develop without express- somes in the same order as they are expressed along A-P ing any of the Hox genes, which, in turn, are expressed axis, a phenomenon referred to as spatial collinearity [2, in the canonical collinear way only in the rudiments of 11–13]. Te clustering of Hox genes in the genome is juvenile worms developing either inside larval body hypothesized as a plesiomorphic feature of Bilateria (e.g., (pilidiophorans) or as the posterior extension of late larva [13]), which, however, went through extensive remod- (enteropneusts) [49, 50]. A somehow similar situation is eling in some evolutionary lineages (e.g., [12, 14–22]. Yet, found in the indirectly developing sea urchin Strongylo- spatial collinearity can be preserved despite a disorgani- centrotus purpuratus, in which only two Hox genes (hox7 zation or split of the ancestral Hox cluster (e.g., [14]), the and hox 11/13b) take part in the larva formation, whereas situation for which the term trans-collinearity was coined the rudiments of adult animal, developing inside the by Duboule [12]. larval body, show collinear expression of fve Hox genes Initially the role of Hox genes has been studied in the (hox7, hox8, hox9/10, hox11/13a and hox11/13b) in the developing embryo of Drosophila melanogaster [23], later extra-axial mesoderm [51, 53–55]. Yet another type of supplemented by the data from other insects, vertebrates the metamorphosis-related Hox genes expression shifts and nematodes [24–26]. Recent advance of molecular is found in scaphopod Antalis entalis in which only the and bioinformatic techniques allowed the investigation of mid-trochophore stage exhibits staggered Hox genes Hox gene expression in the embryos and larvae of several expression, whereas both competent larvae and postmet- non-model species, including, e.g., xenacoelomorphs [16, amorphic juveniles lack spatial collinearity [52]. Some of 27, 28], hemichordates [29], onychophorans [30], tardi- the scaphopod Hox genes partially retain their expression grades [31], rotifers [32], annelids [33–35], mollusks [36– profles throughout metamorphosis (hox2, hox5, lox5), 40], nemerteans [41] and brachiopods [19], essentially whereas other substantially changes their expression increasing knowledge on the diversity of Hox gene-based domains (hox3, lox4, post1, post2) or are expressed only patterning systems in Bilateria. before (hox1) or after (hox4) metamorphosis [52]. It is Many animals are characterized by an indirect life therefore evident that the metamorphosis-related shifts cycle in which embryos develop through a larval stage in Hox gene expression and function vary a lot from one and subsequent metamorphosis, during which the larval animal clade to another, as a result of diverse evolution- body is reshaped into the adult one (e.g., [42, 43]). As lar- ary and developmental processes, which shape the ontog- vae and adults can signifcantly difer in their morphol- eny of each particular group [56]. ogy, the transition process might be quite dramatic and One of the animal groups with a distinct metamor- hence attracted attention of many researchers as one of phosis event are rhynchonelliformean brachiopods, the pivotal moments of the animal development [44–46]. represented by T. transversa for which Schiemann et al. Although the process of metamorphosis has puzzled recently described Hox genes expression in embryos numerous developmental biologists, there are relatively and larvae [19]. Brachiopods, along with phoronids and few studies regarding shifts of Hox gene expression possibly ectoprocts, constitute the clade Lophophorata accompanying it [15, 47–52]. In some animals, both lar- (Fig. 1A, [57, 58]), which, together with, for example, vae and adults show canonical spatial collinearity, which annelids, mollusks, fatworms, nemerteans and rotifers, often correlates with the gradual type of metamorphosis. belongs to a large clade of protostome animals called Tis can be exemplifed by investigated annelid species, in Spiralia (Fig. 1A, [58–61]). Extant brachiopods are tradi- which both life stages exhibit spatial collinearity of most tionally divided into three groups: Rhynchonelliformea, Gąsiorowski and Hejnol EvoDevo (2019) 10:1 Page 3 of 19 Fig. 1 Phylogenetic

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